The Osiris family genes function as novel regulators of the tube maturation process in the Drosophila trachea

Abstract

Drosophila trachea is a premier model to study tube morphogenesis. After the formation of continuous tubes, tube maturation follows. Tracheal tube maturation starts with an apical secretion pulse that deposits extracellular matrix components to form a chitin-based apical luminal matrix (aECM). This aECM is then cleared and followed by the maturation of taenidial folds. Finally, air fills the tubes. Meanwhile, the cellular junctions are maintained to ensure tube integrity. Previous research has identified several key components (ER, Golgi, several endosomes) of protein trafficking pathways that regulate the secretion and clearance of aECM, and the maintenance of cellular junctions. The Osiris (Osi) gene family is located at the Triplo-lethal (Tpl) locus on chromosome 3R 83D4-E3 and exhibits dosage sensitivity. Here, we show that three Osi genes (Osi9, Osi15, Osi19), function redundantly to regulate adherens junction (AJ) maintenance, luminal clearance, taenidial fold formation, tube morphology, and air filling during tube maturation. The localization of Osi proteins in endosomes (Rab7-containing late endosomes, Rab11-containing recycling endosomes, Lamp-containing lysosomes) and the reduction of these endosomes in Osi mutants suggest the possible role of Osi genes in tube maturation through endosome-mediated trafficking. We analyzed tube maturation in zygotic rab11 and rab7 mutants, respectively, to determine whether endosome-mediated trafficking is required. Interestingly, similar tube maturation defects were observed in rab11 but not in rab7 mutants, suggesting the involvement of Rab11-mediated trafficking, but not Rab7-mediated trafficking, in this process. To investigate whether Osi genes regulate tube maturation primarily through the maintenance of Rab11-containing endosomes, we overexpressed rab11 in Osi mutant trachea. Surprisingly, no obvious rescue was observed. Thus, increasing endosome numbers is not sufficient to rescue tube maturation defects in Osi mutants. These results suggest that Osi genes regulate other aspects of endosome-mediated trafficking, or regulate an unknown mechanism that converges or acts in parallel with Rab11-mediated trafficking during tube maturation.

TheivorylncRNA regulates seasonal color patterns in buckeye butterflies

“…A final notable pattern that emerged from the RNA-seq analysis was the strong upregulation of multiple Osiris -family genes in in ivory Δ17kb wings during early pupal development, in terms of fold change, significance, overall read count magnitude, and overall number of Osiris genes (Table S10). This gene family is thought to encode transmembrane transporters, although Osiris genes have not been well characterized outside of tracheal function in Drosophila ( 20 ), and they have not previously been linked to butterfly wing pigmentation. This gene family may provide candidates for future functional assessment.…”

Osirisgene family defines the cuticle nano-patterns ofDrosophila

“…2019a; Scalzotto et al . 2022; Scholl et al . 2023), but no comprehensive mutagenesis of the Osiris gene has been performed before.…”

“…No defect in the cuticle pattern of mechanosensory organs and epidermis was observed, although expression of multiple Osi genes was detected. Genetic redundancy, reported for the tracheal function (Scholl et al . 2023), is a likely reason.…”

“…2018; Scholl et al . 2018, 2023; Scalzotto et al . 2022), no comprehensive analysis of the expression and genetic requirement for Osi family genes has been reported for Drosophila or other insects.…”

Osiris gene family defines the cuticle nanopatterns of Drosophila

“…Although a few studies have addressed the function of specific Osi genes ( Scholl et al . 2018 , 2023 ; Smith et al . 2018 ; Scalzotto et al .…”